Peroxisome proliferator-activated receptor γ agonists potentiate the cytotoxic effect of valproic acid in multiple myeloma cells

British Journal of Haematology

Volumn 147, Issue 5, 2009, Pages 662-671

  Aouali, Nassera ^a   Palissot, Valérie ^a   El Khoury, Victoria ^a   Moussay, Etienne ^a   Janji, Bassam ^a   Pierson, Sandrine ^a   Brons, Nicolaas H C ^a   Kellner, Laurent ^a   Bosseler, Manon ^a   Van Moer, Kris ^a   Berchem, Guy ^a,b  

^a CENTRE HOSPITALIER DE LUXEMBOURG   (Luxembourg)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

Author keywords

Histone deacetylase inhibitors; Multiple myeloma; Pioglitazone; Potentiation

Indexed keywords

CASPASE; HISTONE H3; HISTONE H4; PIOGLITAZONE; VALPROIC ACID;

ACETYLATION; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; EPILEPSY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IC 50; MULTIPLE MYELOMA; MYELOMA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACETYLATION; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CASPASES; CELL CYCLE; CELL DEATH; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; HISTONES; HUMANS; MULTIPLE MYELOMA; PPAR GAMMA; THIAZOLIDINEDIONES; TUMOR CELLS, CULTURED; VALPROIC ACID;

EID: 70449370200     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07902.x     Document Type: Article

References (60)

1. Annicotte, J.S., Iankova, I., Miard, S., Fritz, V., Sarruf, D., Abella, A., Berthe, M.L., Noel, D., Pillon, A., Iborra, F., Dubus, P., Maudelonde, T., Culine, S. Fajas, L. (2006) Peroxisome proliferator-activated receptor gamma regulates E-cadherin expression and inhibits growth and invasion of prostate cancer. Molecular and Cellular Biology, 26, 7561 7574.
2. Atmaca, A., Al-Batran, S.E., Maurer, A., Neumann, A., Heinzel, T., Hentsch, B., Schwarz, S.E., Hovelmann, S., Gottlicher, M., Knuth, A. Jager, E. (2007) Valproic acid (VPA) in patients with refractory advanced cancer: a dose escalating phase I clinical trial. British Journal of Cancer, 97, 177 182.
3. Burton, J.D., Castillo, M.E., Goldenberg, D.M. Blumenthal, R.D. (2007) Peroxisome proliferator-activated receptor-gamma antagonists exhibit potent antiproliferative effects versus many hematopoietic and epithelial cancer cell lines. Anti-Cancer Drugs, 18, 525 534.
4. ten Cate, B., Samplonius, D.F., Bijma, T., de Leij, L.F., Helfrich, W. Bremer, E. (2007) The histone deacetylase inhibitor valproic acid potently augments gemtuzumab ozogamicin-induced apoptosis in acute myeloid leukemic cells. Leukemia, 21, 248 252.
5. Chang, T.H. Szabo, E. (2002) Enhanced growth inhibition by combination differentiation therapy with ligands of peroxisome proliferator-activated receptor-gamma and inhibitors of histone deacetylase in adenocarcinoma of the lung. Clinical Cancer Research, 8, 1206 1212.
6. Chauhan, D., Singh, A., Brahmandam, M., Podar, K., Hideshima, T., Richardson, P., Munshi, N., Palladino, M.A. Anderson, K.C. (2008) Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. Blood, 111, 1654 1664.
7. Cinatl, Jr. J., Cinatl, J., Driever, P.H., Kotchetkov, R., Pouckova, P., Kornhuber, B. Schwabe, D. (1997) Sodium valproate inhibits in vivo growth of human neuroblastoma cells. Anti-Cancer Drugs, 8, 958 963.
8. Coffey, D.C., Kutko, M.C., Glick, R.D., Butler, L.M., Heller, G., Rifkind, R.A., Marks, P.A., Richon, V.M. La Quaglia, M.P. (2001) The histone deacetylase inhibitor, CBHA, inhibits growth of human neuroblastoma xenografts in vivo, alone and synergistically with all-trans retinoic acid. Cancer Research, 61, 3591 3594.
9. Cress, W.D. Seto, E. (2000) Histone deacetylases, transcriptional control, and cancer. Journal of Cellular Physiology, 184, 1 16.
10. Deleu, S., Lemaire, M., Arts, J., Menu, E., Van Valckenborgh, E., King, P., Vande Broek, I., De Raeve, H., Van Camp, B., Croucher, P. Vanderkerken, K. (2009) The effects of JNJ-26481585, a novel hydroxamate-based histone deacetylase inhibitor, on the development of multiple myeloma in the 5T2MM and 5T33MM murine models. Leukemia, doi :.
11. Duenas-Gonzalez, A., Candelaria, M., Perez-Plascencia, C., Perez-Cardenas, E., de la Cruz-Hernandez, E. Herrera, L.A. (2008) Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treatment Reviews, 34, 206 222.
12. Elnemr, A., Ohta, T., Iwata, K., Ninomia, I., Fushida, S., Nishimura, G., Kitagawa, H., Kayahara, M., Yamamoto, M., Terada, T. Miwa, K. (2000) PPARgamma ligand (thiazolidinedione) induces growth arrest and differentiation markers of human pancreatic cancer cells. International Journal of Oncology, 17, 1157 1164.
13. Eucker, J., Bangeroth, K., Zavrski, I., Krebbel, H., Zang, C., Heider, U., Jakob, C., Elstner, E., Possinger, K. Sezer, O. (2004) Ligands of peroxisome proliferator-activated receptor gamma induce apoptosis in multiple myeloma. Anti-Cancer Drugs, 15, 955 960.
14. Garcia-Bates, T.M., Bernstein, S.H. Phipps, R.P. (2008) Peroxisome proliferator-activated receptor gamma overexpression suppresses growth and induces apoptosis in human multiple myeloma cells. Clinical Cancer Research, 14, 6414 6425.
15. Giles, F., Fischer, T., Cortes, J., Garcia-Manero, G., Beck, J., Ravandi, F., Masson, E., Rae, P., Laird, G., Sharma, S., Kantarjian, H., Dugan, M., Albitar, M. Bhalla, K. (2006) A phase I study of intravenous LBH589, a novel cinnamic hydroxamic acid analogue histone deacetylase inhibitor, in patients with refractory hematologic malignancies. Clinical Cancer Research, 12, 4628 4635.
16. Gojo, I., Tidwell, M.L., Greer, J., Takebe, N., Seiter, K., Pochron, M.F., Johnson, B., Sznol, M. Karp, J.E. (2007) Phase I and pharmacokinetic study of Triapine, a potent ribonucleotide reductase inhibitor, in adults with advanced hematologic malignancies. Leukemia Research, 31, 1165 1173.
17. Gottlicher, M. (2004) Valproic acid: an old drug newly discovered as inhibitor of histone deacetylases. Annals of Hematology, 83 (Suppl. 1 S91 S92.
18. Gottlicher, M., Minucci, S., Zhu, P., Kramer, O.H., Schimpf, A., Giavara, S., Sleeman, J.P., Lo Coco, F., Nervi, C., Pelicci, P.G. Heinzel, T. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO Journal, 20, 6969 6978.
19. Gurvich, N., Tsygankova, O.M., Meinkoth, J.L. Klein, P.S. (2004) Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Research, 64, 1079 1086.
20. Hadnagy, A., Beaulieu, R. Balicki, D. (2008) Histone tail modifications and noncanonical functions of histones: perspectives in cancer epigenetics. Molecular Cancer Therapeutics, 7, 740 748.
21. Han, S., Sidell, N., Fisher, P.B. Roman, J. (2004) Up-regulation of p21 gene expression by peroxisome proliferator-activated receptor gamma in human lung carcinoma cells. Clinical Cancer Research, 10, 1911 1919.
22. Hess, A. Iyer, H. (2007) Fisher's combined p-value for detecting differentially expressed genes using Affymetrix expression arrays. BMC Genomics, 8, 96.
23. Insinga, A., Monestiroli, S., Ronzoni, S., Gelmetti, V., Marchesi, F., Viale, A., Altucci, L., Nervi, C., Minucci, S. Pelicci, P.G. (2005) Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nature Medicine, 11, 71 76.
24. Kaiser, M., Zavrski, I., Sterz, J., Jakob, C., Fleissner, C., Kloetzel, P.M., Sezer, O. Heider, U. (2006) The effects of the histone deacetylase inhibitor valproic acid on cell cycle, growth suppression and apoptosis in multiple myeloma. Haematologica, 91, 248 251.
25. Kawa, S., Nikaido, T., Unno, H., Usuda, N., Nakayama, K. Kiyosawa, K. (2002) Growth inhibition and differentiation of pancreatic cancer cell lines by PPAR gamma ligand troglitazone. Pancreas, 24, 1 7.
26. Khan, S.B., Maududi, T., Barton, K., Ayers, J. Alkan, S. (2004) Analysis of histone deacetylase inhibitor, depsipeptide (FR901228), effect on multiple myeloma. British Journal of Haematology, 125, 156 161.
27. Koeffler, H.P. (2003) Peroxisome proliferator-activated receptor gamma and cancers. Clinical Cancer Research, 9, 1 9.
28. Kopelovich, L., Fay, J.R., Glazer, R.I. Crowell, J.A. (2002) Peroxisome proliferator-activated receptor modulators as potential chemopreventive agents. Molecular Cancer Therapeutics, 1, 357 363.
29. Kuendgen, A. Gattermann, N. (2007) Valproic acid for the treatment of myeloid malignancies. Cancer, 110, 943 954.
30. Lagace, D.C. Nachtigal, M.W. (2004) Inhibition of histone deacetylase activity by valproic acid blocks adipogenesis. Journal of Biological Chemistry, 279, 18851 18860.
31. Lagneaux, L., Gillet, N., Stamatopoulos, B., Delforge, A., Dejeneffe, M., Massy, M., Meuleman, N., Kentos, A., Martiat, P., Willems, L. Bron, D. (2007) Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Experimental Hematology, 35, 1527 1537.
32. Latruffe, N. Vamecq, J. (1997) Peroxisome proliferators and peroxisome proliferator activated receptors (PPARs) as regulators of lipid metabolism. Biochimie, 79, 81 94.
33. Lehrmann, H., Pritchard, L.L. Harel-Bellan, A. (2002) Histone acetyltransferases and deacetylases in the control of cell proliferation and differentiation. Advances in Cancer Research, 86, 41 65.
34. Lonial, S. Cavenagh, J. (2009) Emerging combination treatment strategies containing novel agents in newly diagnosed multiple myeloma. British Journal of Haematology, 145, 681 708.
35. Loscher, W. (1993) Effects of the antiepileptic drug valproate on metabolism and function of inhibitory and excitatory amino acids in the brain. Neurochemical Research, 18, 485 502.
36. Loscher, W. (1999) Valproate: a reappraisal of its pharmacodynamic properties and mechanisms of action. Progress in Neurobiology, 58, 31 59.
37. Maggio, S.C., Rosato, R.R., Kramer, L.B., Dai, Y., Rahmani, M., Paik, D.S., Czarnik, A.C., Payne, S.G., Spiegel, S. Grant, S. (2004) The histone deacetylase inhibitor MS-275 interacts synergistically with fludarabine to induce apoptosis in human leukemia cells. Cancer Research, 64, 2590 2600.
38. Marks, P., Rifkind, R.A., Richon, V.M., Breslow, R., Miller, T. Kelly, W.K. (2001) Histone deacetylases and cancer: causes and therapies. Nature Reviews. Cancer, 1, 194 202.
39. Matsuo, Y., Drexler, H.G., Harashima, A., Okochi, A., Hasegawa, A., Kojima, K. Orita, K. (2004) Induction of CD28 on the new myeloma cell line MOLP-8 with t(11;14)(q13;q32) expressing delta/lambda type immunoglobulin. Leukemia Research, 28, 869 877.
40. Matsuyama, M. Yoshimura, R. (2008) Peroxisome Proliferator-Activated Receptor-gamma is a Potent Target for Prevention and Treatment in Human Prostate and Testicular Cancer. PPAR Research, 2008, 249849.
41. Mitsiades, C.S., Hayden, P.J., Anderson, K.C. Richardson, P.G. (2007) From the bench to the bedside: emerging new treatments in multiple myeloma. Best Practice & Research Clinical Haematology, 20, 797 816.
42. Munster, P., Marchion, D., Bicaku, E., Lacevic, M., Kim, J., Centeno, B., Daud, A., Neuger, A., Minton, S. Sullivan, D. (2009) Clinical and biological effects of valproic acid as a histone deacetylase inhibitor on tumor and surrogate tissues: phase I/II trial of valproic acid and epirubicin/FEC. Clinical Cancer Research, 15, 2488 2496.
43. Neri, P., Tagliaferri, P., Di Martino, M.T., Calimeri, T., Amodio, N., Bulotta, A., Ventura, M., Eramo, P.O., Viscomi, C., Arbitrio, M., Rossi, M., Caraglia, M., Munshi, N.C., Anderson, K.C. Tassone, P. (2008) In vivo anti-myeloma activity and modulation of gene expression profile induced by valproic acid, a histone deacetylase inhibitor. British Journal of Haematology, 143, 520 531.
44. Ocio, E.M., Mateos, M.V., Maiso, P., Pandiella, A. San-Miguel, J.F. (2008) New drugs in multiple myeloma: mechanisms of action and phase I/II clinical findings. The Lancet Oncology, 9, 1157 1165.
45. Park, J., Ayyappan, V., Bae, E.K., Lee, C., Kim, B.S., Kim, B.K., Lee, Y.Y., Ahn, K.S. Yoon, S.S. (2008) Curcumin in combination with bortezomib synergistically induced apoptosis in human multiple myeloma U266 cells. Molecular Oncology, 2, 317 326.
46. Ray, D.M., Bernstein, S.H. Phipps, R.P. (2004) Human multiple myeloma cells express peroxisome proliferator-activated receptor gamma and undergo apoptosis upon exposure to PPARgamma ligands. Clinical Immunology, 113, 203 213.
47. Richardson, P., Mitsiades, C., Colson, K., Reilly, E., McBride, L., Chiao, J., Sun, L., Ricker, J., Rizvi, S., Oerth, C., Atkins, B., Fearen, I., Anderson, K. Siegel, D. (2008) Phase I trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) in patients with advanced multiple myeloma. Leukaemia & Lymphoma, 49, 502 507. (Pubitemid 351298334)
48. Rosen, E.D., Hsu, C.H., Wang, X., Sakai, S., Freeman, M.W., Gonzalez, F.J. Spiegelman, B.M. (2002) C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes and Development, 16, 22 26.
49. Sarraf, P., Mueller, E., Jones, D., King, F.J., DeAngelo, D.J., Partridge, J.B., Holden, S.A., Chen, L.B., Singer, S., Fletcher, C. Spiegelman, B.M. (1998) Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nature Medicine, 4, 1046 1052.
50. Schmidt, M., Lu, Y., Liu, B., Fang, M., Mendelsohn, J. Fan, Z. (2000) Differential modulation of paclitaxel-mediated apoptosis by p21Waf1 and p27Kip1. Oncogene, 19, 2423 2429.
51. Schwartz, C., Palissot, V., Aouali, N., Wack, S., Brons, N.H., Leners, B., Bosseler, M. Berchem, G. (2007) Valproic acid induces non-apoptotic cell death mechanisms in multiple myeloma cell lines. International Journal of Oncology, 30, 573 582.
52. Sears, D.D., Hsiao, A., Ofrecio, J.M., Chapman, J., He, W. Olefsky, J.M. (2007) Selective modulation of promoter recruitment and transcriptional activity of PPARgamma. Biochemical and Biophysical Research Communications, 364, 515 521.
53. Shen, W.T., Wong, T.S., Chung, W.Y., Wong, M.G., Kebebew, E., Duh, Q.Y. Clark, O.H. (2005) Valproic acid inhibits growth, induces apoptosis, and modulates apoptosis-regulatory and differentiation gene expression in human thyroid cancer cells. Surgery, 138, 979 984.
54. Stadtmauer, E.A., Weber, D.M., Niesvizky, R., Belch, A., Prince, M.H., San Miguel, J.F., Facon, T., Olesnyckyj, M., Yu, Z., Zeldis, J.B., Knight, R.D. Dimopoulos, M.A. (2009) Lenalidomide in combination with dexamethasone at first relapse in comparison with its use as later salvage therapy in relapsed or refractory multiple myeloma. European Journal of Haematology, 82, 426 432.
55. Timmermann, S., Lehrmann, H., Polesskaya, A. Harel-Bellan, A. (2001) Histone acetylation and disease. Cellular and Molecular Life Sciences, 58, 728 736.
56. Wang, T., Xu, J., Yu, X., Yang, R. Han, Z.C. (2006) Peroxisome proliferator-activated receptor gamma in malignant diseases. Critical Reviews in Oncology/hematology, 58, 1 14.
57. Warrell, Jr., R.P., He, L.Z., Richon, V., Calleja, E. Pandolfi, P.P. (1998) Therapeutic targeting of transcription in acute promyelocytic leukemia by use of an inhibitor of histone deacetylase. Journal of the National Cancer Institute, 90, 1621 1625.
58. Xu, W.S., Parmigiani, R.B. Marks, P.A. (2007) Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene, 26, 5541 5552.
59. Yeow, W.S., Ziauddin, M.F., Maxhimer, J.B., Shamimi-Noori, S., Baras, A., Chua, A., Schrump, D.S. Nguyen, D.M. (2006) Potentiation of the anticancer effect of valproic acid, an antiepileptic agent with histone deacetylase inhibitory activity, by the kinase inhibitor Staurosporine or its clinically relevant analogue UCN-01. British Journal of Cancer, 94, 1436 1445.
60. Yoshida, M., Kijima, M., Akita, M. Beppu, T. (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. Journal of Biological Chemistry, 265, 17174 17179.